A Thermococci-to-Clostridia Pathway for the Evolution of the Bacteria Domain
Main Article Content
Abstract
With the identification of an archaeal Last Universal Common Ancestor (LUCA) related to the archaeon Methanopyrus, the origin of Bacteria became a choice between autonomic development versus descent from Archaea. The similarity bitscores between paralogous valyl-tRNA synthetase (VARS) and isoleucyl-tRNA synthetase (IARS) suggest that the five oldest bacteria were Mahella australiensis, Thermincola potens, Halobacteroides halobius, Desulfosporosinus orientis and Caldicellulosiruptor lactoaceticus, which were all Clostridia species and hydrogen producers. A search for archaea that could be a candidate Progenitor of Bacteria endowed with an Emden-Myerhof-Parnas type glycolytic pathway and a clostridial-like dark-fermentation mechanism for generating hydrogen pointed to such a role for the anaerobic chemoorganotroph Thermococci, which were known to engage in rapid evolutionary changes at high-biodiversity sites abundant in sugars and other small molecular substrates, and constitute together with Clostridia the two most powerful microbial generators of hydrogen. Moreover, two-domain maximum-likelihood and maximum-parsimony phylogenetic trees for VARS showed that Thermococci and Clostridia formed sister clades on both trees, and close similarity was evident between their VARS sequences, which were consistent with kinship between them. On this basis, it was proposed that the Bacteria domain emerged from a thermocococal or thermococcal-like Progenitor of Bacteria possibly at some high-biodiversity site, through the formation of a Thermincola-proximal Last Bacterial Common Ancestor (LBCA).
Keywords:
Thermococci, Clostridia, Thermococci-to-Clostridia Pathway, Evolution of the Bacteria, Bacteria
Article Details
How to Cite
WONG, Tze-Fei; CHAN, Chung-Kwon; XUE, Hong.
A Thermococci-to-Clostridia Pathway for the Evolution of the Bacteria Domain.
Medical Research Archives, [S.l.], v. 11, n. 12, jan. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4878>. Date accessed: 16 may 2024.
doi: https://doi.org/10.18103/mra.v11i12.4878.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990; 87(12):4576-4579. doi:10.1073/pnas.87.12.4576.
2. Xue H, Tong KL, Marck C, Grosjean H, Wong JTF. Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. Gene. 2003; 310:59-66. doi:10.1016/s0378- 1119 (03)00552-3
3. Wong JTF, Ng SK, Mat WK, Hu T, Xue H. Coevolution theory of the genetic code at age forty: pathway to translation and synthetic life. Life. 2016;6(1):12. doi:10.3390/life6010012.
4. Blank CE. Low rates of lateral gene transfer among metabolic genes define the evolving biogeochemical niches of archaea through deep time. Archaea 2012; 2012: 23. doi: 10.1155/2012/843539.
5. Weiss MC, Preiner M, Xavier JC, Zimorski V, Martin WF. The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genet. 2018;14(8) :e1007518.doi:10.1371/journal.pgen.1007518.
6. Schwartz RM, Dayhoff MO. Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science. 1978; 199(4327):395-403. doi:10.1126/science.202030
7. Long X, Xue H, Wong JT. Descent of bacteria and eukarya from an archaeal root of life. Evol Bioinform. 2020;16:117693432 0908267. doi:10.1177/1176934320908267
8. Wong JT, Chan CK, Long X, Xue H. An ectosymbiosis-based mechanism of eukaryogenesis. Med Res Arch 2023; 11(1). Doi.org/10.18103/mro.v11i1.3365.
9. Bocchetta M, Gribaldo S, Sanangelantoni A, Cammarano P. Phylogenetic depth of the bacterial genera Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J Mol Evol. 2000; 50(4):366-380. doi:10.1007/s002399910040
10. Brochier C, Philippe H. Phylogeny: a non-hyperthermophlic ancestor for bacteria. Nature 2002; 447 (6886):244.doi:10.1038/ 417244a.
11. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science. 2006; 311(5765): 1283-1287. Brochierdoi:10.1126/science.1123061
12. Coleman GA, Davín AA, Mahendrarajah TA, et al. A rooted phylogeny resolves early bacterial evolution. Science. 2021;372(6542) :eabe0511. doi:10.1126/science.abe0511
13. Xavier JC, Gerhards RE, Wimmer JLE, Brueckner J, Tria FDK, Martin WF. The metabolic network of the last bacterial common ancestor. Commun Biol. 2021; 4(1):413. doi:10.1038/s42003-021-01918-4
14. Doolittle WF, Bapteste E. Pattern pluralism and the Tree of Life hypothesis. Proc Natl Acad Sci U S A. 2007;104(7):2043-2049. doi:10.1073/pnas.0610699104
15. Blais C, Archibald JM. The past, present and future of the tree of life. Curr Biol. 2021; 31(7):R314-R321. doi:10.1016/j.cub.2021.02.052
16. Harish A, Kurland CG. Empirical genome evolution models root the tree of life. Biochimie. 2017;138:137-155. doi:10.1016/j. biochi.2017.04.014
17. Estrada A, Suárez-Díaz E, Becerra A. Reconstructing the Last Common Ancestor: epistemological and empirical challenges. Acta Biotheor 2022; 70(2):15. doi:10.1007/s1 0441-022-09439-1
18. Minh BQ, Lanfear R, Ly-Trong N, Trifinopoulos J, Schrempf D et al, IQ-TREE version 2.2.0 Tutorials and manual phylogenomic software by maximum likelihood. 2022; 37(5). doi: 10.1093/molbev/ msaa015
19. Swoford, D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0b10 win32. Sunderland. MA: Sinauer.
20. Salinas BM, Fardeau ML, Thomas P, Cayol JL, Patel BKC, Ollivier B. Mahella australiensis gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from an Australian oil well. Int J Syst Evol Microbiol. 2004; 54(Pt 6):2169-2173. doi:10. 1099/ijs.0.02926-00.
21. Fu, Q., Kobayashi, H., Kuramochi, Y., Xu, J., Wakayama, T. et al, 2013. Bioelectrochemical analyses of a thermophilic biocathode catalyzing sustainable hydrogen production. Int. J. Hydrogen Energy 38(35), 15638-45.
22. Sokolova TG, Kostrikina NA, Chernyh NA, Kolganova TV, Tourova TP, Bonch-Osmolovskaya EA. Thermincola carboxydiphila gen. nov., sp. nov., a novel anaerobic, carboxydotrophic, hydrogenogenic bacterium from a hot spring of the Lake Baikal area. Int J Syst Evol Microbiol. 2005; 55(Pt 5):2069-2073. doi:10.1 099/ijs.0.63299-0.
23. Oren A, Weisburg WG, Kessel M, Woese CR. Halobacteroides halobius gen. nov., sp. nov., a moderately halophilic anaerobic bacterium from the bottom sediments of the Dead Sea. Syst Appl Microbiol 1984;5(1): 58-70. doi:10.1016/S0723-2020(84)80051-X.
24. Agostino V, Lenic A, Bardl B, et al. Electrophysiology of the facultative autotrophic bacterium Desulfosporosinus orientis. Front Bioeng Biotechnol. 2020;8:457. doi:10.3389/fbioe.2020.00457.
25. Mladenovska Z, Mathrani IM, Ahring BK. Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an extremely thermophilic, cellulolytic, anaerobic bacterium. Arch Microbiol 1995;163:223-230. doi:10.1007/BF00305357
26. van Niel EW. Biological processes for hydrogen production. Adv Biochem Eng Biotechnol. 2016; 156:155-193. doi:10.1007/ 10_2016_11
27. Bräsen C, Esser D, Rauch B, Siebers B. Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol Mol Biol Rev. 2014; 78(1):89-175. doi:10.1128/MMBR.00041-13
28. Verhees CH, Kengen SW, Tuininga JE, et al. The unique features of glycolytic pathways in Archaea. Biochem J. 2003;375(Pt 2):231-246. doi:10.1042/BJ20021472
29. Verhaart MR, Bielen AA, van der Oost J, Stams AJ, Kengen SW. Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal. Environ Technol 2010; 31(8-9):993-1003. doi:10.1080/ 09593331003710244
30. Shakir NA, Bibi T, Aslam M, Rashid N. Biochemical characterization of a highly active ADP-dependent phosphofructokinase from Thermococcus kodakarensis. J Biosci Bioeng. 2020; 129(1):6-15. doi:10.1016/j.jbiosc.2019.06.014
31. Kobayashi, T. Genus I. Thermococcus. (2001) ‘The archaea and deeply branching and phototrophic bacteria, eds’, in Bergey’s Manual of systematic bacteriology. 2nd edn, pp. 342–346.
32. Fiala G, Stetter KO. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100℃. Arch Microbiol 1986;145:56-61. doi: 10.1007/BF00413027
33. Einsele G, Gieskes JM, Curray J, et al. Intrusion of basaltic sills into highly porous sediments, and resulting hydrothermal activity. Nature 1980;283:441-445. doi:10. 1038/283441a0
34. Simoneit BRT, Lonsdale PF. Hydrothermal petroleum in mineralized mounds at the seabed of Guaymas Basin. Nature 1982;5(1-2):29-40. doi:10.1038/295198a0
35. McKay L, Klokman VW, Mendlovitz HP, et al. Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California. Environ Microbiol Rep 2016;8 (1):150-161. doi:10.1111/1758-2229.12365
36. Liu L, Wang F, Xu J, Xiao X. Molecular diversity of Thermococcales isolated from Guaymas Basin hydrothermal vents. Acta Oceanol Sin 2013;32:75-81. doi:10.1007/s1 3131-013-0323-3
37. Dombrowski N, Teske AP, Baker BJ. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat Commun. 2018; 9(1):4999. doi:10.1038/s41467-018-07418-0
38. Collins MD, Lawson PA, Willems A, et al. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol. 1994; 44(4):812-826. doi:10.1099/00207713-44-4-812.
39. Bao Q, Tian Y, Li W, Xu Z, Yang H. A complete sequence of the T. tencongensis genome. Genome Res 2002; 12(5):689-700. Doi:10.1101/gr.219302
43. Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet. 2015;16(8):472-482. doi: 10.1038/nrg3962.
41. Reed CJ, Lewis H, Trejo E, Winston V, Evilia C. Protein adaptations in archaeal extremophiles. Archea.2013; 2013:373275. doi :10.1155/2013/373275
2. Xue H, Tong KL, Marck C, Grosjean H, Wong JTF. Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. Gene. 2003; 310:59-66. doi:10.1016/s0378- 1119 (03)00552-3
3. Wong JTF, Ng SK, Mat WK, Hu T, Xue H. Coevolution theory of the genetic code at age forty: pathway to translation and synthetic life. Life. 2016;6(1):12. doi:10.3390/life6010012.
4. Blank CE. Low rates of lateral gene transfer among metabolic genes define the evolving biogeochemical niches of archaea through deep time. Archaea 2012; 2012: 23. doi: 10.1155/2012/843539.
5. Weiss MC, Preiner M, Xavier JC, Zimorski V, Martin WF. The last universal common ancestor between ancient Earth chemistry and the onset of genetics. PLoS Genet. 2018;14(8) :e1007518.doi:10.1371/journal.pgen.1007518.
6. Schwartz RM, Dayhoff MO. Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science. 1978; 199(4327):395-403. doi:10.1126/science.202030
7. Long X, Xue H, Wong JT. Descent of bacteria and eukarya from an archaeal root of life. Evol Bioinform. 2020;16:117693432 0908267. doi:10.1177/1176934320908267
8. Wong JT, Chan CK, Long X, Xue H. An ectosymbiosis-based mechanism of eukaryogenesis. Med Res Arch 2023; 11(1). Doi.org/10.18103/mro.v11i1.3365.
9. Bocchetta M, Gribaldo S, Sanangelantoni A, Cammarano P. Phylogenetic depth of the bacterial genera Aquifex and Thermotoga inferred from analysis of ribosomal protein, elongation factor, and RNA polymerase subunit sequences. J Mol Evol. 2000; 50(4):366-380. doi:10.1007/s002399910040
10. Brochier C, Philippe H. Phylogeny: a non-hyperthermophlic ancestor for bacteria. Nature 2002; 447 (6886):244.doi:10.1038/ 417244a.
11. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science. 2006; 311(5765): 1283-1287. Brochierdoi:10.1126/science.1123061
12. Coleman GA, Davín AA, Mahendrarajah TA, et al. A rooted phylogeny resolves early bacterial evolution. Science. 2021;372(6542) :eabe0511. doi:10.1126/science.abe0511
13. Xavier JC, Gerhards RE, Wimmer JLE, Brueckner J, Tria FDK, Martin WF. The metabolic network of the last bacterial common ancestor. Commun Biol. 2021; 4(1):413. doi:10.1038/s42003-021-01918-4
14. Doolittle WF, Bapteste E. Pattern pluralism and the Tree of Life hypothesis. Proc Natl Acad Sci U S A. 2007;104(7):2043-2049. doi:10.1073/pnas.0610699104
15. Blais C, Archibald JM. The past, present and future of the tree of life. Curr Biol. 2021; 31(7):R314-R321. doi:10.1016/j.cub.2021.02.052
16. Harish A, Kurland CG. Empirical genome evolution models root the tree of life. Biochimie. 2017;138:137-155. doi:10.1016/j. biochi.2017.04.014
17. Estrada A, Suárez-Díaz E, Becerra A. Reconstructing the Last Common Ancestor: epistemological and empirical challenges. Acta Biotheor 2022; 70(2):15. doi:10.1007/s1 0441-022-09439-1
18. Minh BQ, Lanfear R, Ly-Trong N, Trifinopoulos J, Schrempf D et al, IQ-TREE version 2.2.0 Tutorials and manual phylogenomic software by maximum likelihood. 2022; 37(5). doi: 10.1093/molbev/ msaa015
19. Swoford, D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (* and other methods), version 4.0b10 win32. Sunderland. MA: Sinauer.
20. Salinas BM, Fardeau ML, Thomas P, Cayol JL, Patel BKC, Ollivier B. Mahella australiensis gen. nov., sp. nov., a moderately thermophilic anaerobic bacterium isolated from an Australian oil well. Int J Syst Evol Microbiol. 2004; 54(Pt 6):2169-2173. doi:10. 1099/ijs.0.02926-00.
21. Fu, Q., Kobayashi, H., Kuramochi, Y., Xu, J., Wakayama, T. et al, 2013. Bioelectrochemical analyses of a thermophilic biocathode catalyzing sustainable hydrogen production. Int. J. Hydrogen Energy 38(35), 15638-45.
22. Sokolova TG, Kostrikina NA, Chernyh NA, Kolganova TV, Tourova TP, Bonch-Osmolovskaya EA. Thermincola carboxydiphila gen. nov., sp. nov., a novel anaerobic, carboxydotrophic, hydrogenogenic bacterium from a hot spring of the Lake Baikal area. Int J Syst Evol Microbiol. 2005; 55(Pt 5):2069-2073. doi:10.1 099/ijs.0.63299-0.
23. Oren A, Weisburg WG, Kessel M, Woese CR. Halobacteroides halobius gen. nov., sp. nov., a moderately halophilic anaerobic bacterium from the bottom sediments of the Dead Sea. Syst Appl Microbiol 1984;5(1): 58-70. doi:10.1016/S0723-2020(84)80051-X.
24. Agostino V, Lenic A, Bardl B, et al. Electrophysiology of the facultative autotrophic bacterium Desulfosporosinus orientis. Front Bioeng Biotechnol. 2020;8:457. doi:10.3389/fbioe.2020.00457.
25. Mladenovska Z, Mathrani IM, Ahring BK. Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an extremely thermophilic, cellulolytic, anaerobic bacterium. Arch Microbiol 1995;163:223-230. doi:10.1007/BF00305357
26. van Niel EW. Biological processes for hydrogen production. Adv Biochem Eng Biotechnol. 2016; 156:155-193. doi:10.1007/ 10_2016_11
27. Bräsen C, Esser D, Rauch B, Siebers B. Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol Mol Biol Rev. 2014; 78(1):89-175. doi:10.1128/MMBR.00041-13
28. Verhees CH, Kengen SW, Tuininga JE, et al. The unique features of glycolytic pathways in Archaea. Biochem J. 2003;375(Pt 2):231-246. doi:10.1042/BJ20021472
29. Verhaart MR, Bielen AA, van der Oost J, Stams AJ, Kengen SW. Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal. Environ Technol 2010; 31(8-9):993-1003. doi:10.1080/ 09593331003710244
30. Shakir NA, Bibi T, Aslam M, Rashid N. Biochemical characterization of a highly active ADP-dependent phosphofructokinase from Thermococcus kodakarensis. J Biosci Bioeng. 2020; 129(1):6-15. doi:10.1016/j.jbiosc.2019.06.014
31. Kobayashi, T. Genus I. Thermococcus. (2001) ‘The archaea and deeply branching and phototrophic bacteria, eds’, in Bergey’s Manual of systematic bacteriology. 2nd edn, pp. 342–346.
32. Fiala G, Stetter KO. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100℃. Arch Microbiol 1986;145:56-61. doi: 10.1007/BF00413027
33. Einsele G, Gieskes JM, Curray J, et al. Intrusion of basaltic sills into highly porous sediments, and resulting hydrothermal activity. Nature 1980;283:441-445. doi:10. 1038/283441a0
34. Simoneit BRT, Lonsdale PF. Hydrothermal petroleum in mineralized mounds at the seabed of Guaymas Basin. Nature 1982;5(1-2):29-40. doi:10.1038/295198a0
35. McKay L, Klokman VW, Mendlovitz HP, et al. Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California. Environ Microbiol Rep 2016;8 (1):150-161. doi:10.1111/1758-2229.12365
36. Liu L, Wang F, Xu J, Xiao X. Molecular diversity of Thermococcales isolated from Guaymas Basin hydrothermal vents. Acta Oceanol Sin 2013;32:75-81. doi:10.1007/s1 3131-013-0323-3
37. Dombrowski N, Teske AP, Baker BJ. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat Commun. 2018; 9(1):4999. doi:10.1038/s41467-018-07418-0
38. Collins MD, Lawson PA, Willems A, et al. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol. 1994; 44(4):812-826. doi:10.1099/00207713-44-4-812.
39. Bao Q, Tian Y, Li W, Xu Z, Yang H. A complete sequence of the T. tencongensis genome. Genome Res 2002; 12(5):689-700. Doi:10.1101/gr.219302
43. Soucy SM, Huang J, Gogarten JP. Horizontal gene transfer: building the web of life. Nat Rev Genet. 2015;16(8):472-482. doi: 10.1038/nrg3962.
41. Reed CJ, Lewis H, Trejo E, Winston V, Evilia C. Protein adaptations in archaeal extremophiles. Archea.2013; 2013:373275. doi :10.1155/2013/373275