Investigation of tRNA-based relatedness within the Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) superphylum: a comparative analysis.
Evolutionary analysis
Last universal common ancestor of life (LUCA)
RNA biology
Ribozymes
Threonylcarbamoyl adenosine (t6A)
tRNA
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
02 Nov 2023
02 Nov 2023
Historique:
received:
21
08
2023
accepted:
27
09
2023
revised:
23
09
2023
medline:
6
11
2023
pubmed:
2
11
2023
entrez:
2
11
2023
Statut:
epublish
Résumé
The PVC superphylum is a diverse group of prokaryotes that require stringent growth conditions. RNA is a fascinating molecule to find evolutionary relatedness according to the RNA World Hypothesis. We conducted tRNA gene analysis to find evolutionary relationships in the PVC phyla. The analysis of genomic data (P = 9, V = 4, C = 8) revealed that the number of tRNA genes varied from 28 to 90 in Planctomycetes and Chlamydia, respectively. Verrucomicrobia has whole genomes and the longest scaffold (3 + 1), with tRNA genes ranging from 49 to 53 in whole genomes and 4 in the longest scaffold. Most tRNAs in the E. coli genome clustered with homologs, but approximately 43% clustered with tRNAs encoding different amino acids. Planctomyces, Akkermansia, Isosphaera, and Chlamydia were similar to E. coli tRNAs. In a phylum, tRNAs coding for different amino acids clustered at a range of 8 to 10%. Further analysis of these tRNAs showed sequence similarity with Cyanobacteria, Proteobacteria, Viridiplantae, Ascomycota and Basidiomycota (Eukaryota). This indicates the possibility of horizontal gene transfer or, otherwise, a different origin of tRNA in PVC bacteria. Hence, this work proves its importance for determining evolutionary relatedness and potentially identifying bacteria using tRNA. Thus, the analysis of these tRNAs indicates that primitive RNA may have served as the genetic material of LUCA before being replaced by DNA. A quantitative analysis is required to test these possibilities that relate the evolutionary significance of tRNA to the origin of life.
Identifiants
pubmed: 37917352
doi: 10.1007/s00203-023-03694-7
pii: 10.1007/s00203-023-03694-7
doi:
Substances chimiques
RNA, Transfer
9014-25-9
Amino Acids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
366Subventions
Organisme : University Grants Commission
ID : PDFSS-2013-14-ST-MAH-4350
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York (ISBN-10: 0-8153-3218-1, 0-8153-4072-9)
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
doi: 10.1016/S0022-2836(05)80360-2
pubmed: 2231712
Athavale SS, Petrov AS, Hsiao C, Watkins D, Prickett CD, Gossett JJ, Lie L, Bowman JC, O’Neill E, Bernier CR, Hud NV, Wartell RM, Harvey SC (2012) RNA folding and catalysis mediated by iron (II). PLoS ONE 7(5):e38024. https://doi.org/10.1371/journal.pone.0038024
doi: 10.1371/journal.pone.0038024
pubmed: 22701543
pmcid: 3365117
Boedeker C, Schuler M, Reintjes G, Jeske O, van Teeseling MCF, Jogler M, Rast P, Borchert D, Devos DP, Kucklick M, Schaffer M, Kolter R, van Niftrik L, Engelmann S, Amann R, Rohde M, Engelhardt H, Jogler C (2017) Determining the bacterial cell biology of Planctomycetes. Nat Commun 8:14853. https://doi.org/10.1038/ncomms14853
doi: 10.1038/ncomms14853
pubmed: 28393831
pmcid: 5394234
Bordin N, González-Sánchez JC, Devos DP (2018) PVCbase: an integrated web resource for the PVC bacterial proteomes. Database (oxford) 2018:bay042. https://doi.org/10.1093/database/bay042
doi: 10.1093/database/bay042
pubmed: 29718141
Bowman JC, Lenz TK, Hud NV, Williams LD (2012) Cations in charge: magnesium ions in RNA folding and catalysis. Curr Opin Struct Biol 22:262–272. https://doi.org/10.1016/j.sbi.2012.04.006
doi: 10.1016/j.sbi.2012.04.006
pubmed: 22595008
Brown TA (2002) Genomes, 2nd edn. Oxford: Wiley-Liss; Chapter 7, Understanding a genome sequence. Available from: https://www.ncbi.nlm.nih.gov/books/NBK21136/ . Accessed 23 Sept 2023
Budd A, Devos DP (2012) Evaluating the evolutionary origins of unexpected character distributions within the bacterial Planctomycetes−Verrucomicrobia−Chlamydiae superphylum. Front Microbiol 3:401. https://doi.org/10.3389/fmicb.2012.00401
doi: 10.3389/fmicb.2012.00401
pubmed: 23189077
pmcid: 3505017
Chan PP, Lowe TM (2019) tRNAscan-SE: searching for tRNA genes in genomic sequences. Methods Mol Biol 1962:1–14
doi: 10.1007/978-1-4939-9173-0_1
pubmed: 31020551
pmcid: 6768409
Cooper GM (2000) The cell: a molecular approach, 2nd edn. Sinauer Associates, Sunderland (MA) (NCBI Bookshelf ID: NBK9841)
Crichton RR (2008) Iron: essential for almost all life. Biol Inorg Chem. https://doi.org/10.1016/B978-044452740-0.50013-2
doi: 10.1016/B978-044452740-0.50013-2
Daffonchio D, Borin S, Frova G, Manachini PL, Sorlini C (1998) PCR fingerprinting of whole genomes: the spacers between the 16 s and 23 s rRNA genes and of intergenic tRNA gene regions reveal a different intraspecific genomic variability of Bacillus cereus and Bacillus licheniforrnis. Int J Syst Evol Microbiol 48:107–116. https://doi.org/10.1099/00207713-48-1-107
doi: 10.1099/00207713-48-1-107
Devos DP, Jogler C, Fuerst JA (2013) The 1st EMBO workshop on PVC bacteria-Planctomycetes–Verrucomicrobia–Chlamydiae superphylum: exceptions to the bacterial definition? Antonie Van Leeuwenhoek 104:443–449. https://doi.org/10.1007/s10482-013-0026-y
doi: 10.1007/s10482-013-0026-y
pubmed: 24052364
Erlich Y, Zielinski D (2017) DNA Fountain enables a robust and efficient storage architecture. Science 355(6328):950–954. https://doi.org/10.1126/science.aaj2038
Forterre P (2015) The universal tree of life: an update. Front Microbiol 6:717. https://doi.org/10.3389/fmicb.2015.00717
doi: 10.3389/fmicb.2015.00717
pubmed: 26257711
pmcid: 4508532
Fuerst JA (2013) The PVC superphylum: exceptions to the bacterial definition?”. Antonie Van Leeuwenhoek 104(4):451–466. https://doi.org/10.1007/s10482-013-9986-1
doi: 10.1007/s10482-013-9986-1
pubmed: 23912444
Fujishima K, Kanai A (2014) tRNA gene diversity in the three domains of life. Front Genet 5:142. https://doi.org/10.3389/fgene.2014.00142
doi: 10.3389/fgene.2014.00142
pubmed: 24904642
pmcid: 4033280
Giegé R (2008) Toward a more complete view of tRNA biology. Nat Struct Mol Biol 15(10):1007–1014. https://doi.org/10.1038/nsmb.1498
doi: 10.1038/nsmb.1498
pubmed: 18836497
Gupta RS, Bhandari V, Naushad HS (2012) Molecular signatures for the PVC clade (Planctomycetes, Verrucomicrobia, Chlamydiae, and Lentisphaerae) of bacteria provide insights into their evolutionary relationships. Front Microbiol 3:327. https://doi.org/10.3389/fmicb.2012.00327
doi: 10.3389/fmicb.2012.00327
pubmed: 23060863
pmcid: 3444138
Gurtler V, Mayall BC (2001) Genomic approaches to typing, taxonomy and evolution of bacterial isolates. Int J Syst Evol Microbiol 51:3–16. https://doi.org/10.1099/00207713-51-1-3
doi: 10.1099/00207713-51-1-3
pubmed: 11211268
Hazen RM, Papineau D, Leeker WB, Downs RT, Ferry JM, McCoy TJ, Sverjensky DA, Yang H (2008) Mineral evolution. Am Miner 93:1693–1720. https://doi.org/10.2138/am.2008.2955
doi: 10.2138/am.2008.2955
Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD (2013) The origin of RNA and “My grandfather’s axe.” Chem Biol 20:466–474. https://doi.org/10.1016/j.chembiol.2013.03.012
doi: 10.1016/j.chembiol.2013.03.012
pubmed: 23601635
Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K, Suzuki Y, Dudek N, Relman DA, Finstad KM, Amundson R, Thomas BC, Banfield JF (2016) A new view of the tree of life. Nat Microbiol 1:16048. https://doi.org/10.1038/nmicrobiol.2016.48
doi: 10.1038/nmicrobiol.2016.48
pubmed: 27572647
Joyce GF (1989) RNA evolution and the origin of life. Nature 338:217–224. https://doi.org/10.1038/338217a0
doi: 10.1038/338217a0
pubmed: 2466202
Katz A, Elgamal S, Rajkovic A, Ibba M (2016) Non-canonical roles of tRNAs and tRNA mimics in bacterial cell biology. Mol Microbiol 101(4):545–558. https://doi.org/10.1111/mmi.13419
doi: 10.1111/mmi.13419
pubmed: 27169680
pmcid: 5003029
Kim Y, Kowiatek B, Opron K, Burton ZF (2018) Type-II tRNAs and evolution of translation systems and the genetic code. Int J Mol Sci 19:3275. https://doi.org/10.3390/ijms19103275
doi: 10.3390/ijms19103275
pubmed: 30360357
pmcid: 6214036
Kim Y, Opron K, Burton ZF (2019) A tRNA- and anticodon-centric view of the evolution of aminoacyl-tRNA synthetases, tRNAomes, and the genetic Code. Life 9(2):37. https://doi.org/10.3390/life9020037
doi: 10.3390/life9020037
pubmed: 31060233
pmcid: 6616430
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306. https://doi.org/10.1093/bib/bbn017
doi: 10.1093/bib/bbn017
pubmed: 18417537
Lagkouvardos I, Jehl MA, Rattei T, Horn M (2014) Signature protein of the PVC superphylum. Appl Environ Microbiol 80(2):440–445. https://doi.org/10.1128/AEM.02655-13
doi: 10.1128/AEM.02655-13
pubmed: 24185849
pmcid: 3911108
Lee KC, Webb RI, Janssen PH, Sangwan P, Romeo T, Staley JT, Fuerst JA (2009) Phylum Verrucomicrobia representatives share a compartmentalized cell plan with members of bacterial phylum Planctomycetes. BMC Microbiol 9:5. https://doi.org/10.1186/1471-2180-9-5
doi: 10.1186/1471-2180-9-5
pubmed: 19133117
pmcid: 2647929
Lonhiennea TGA, Sagulenko E, Webb RI, Lee KC, Franke J, Devose DP, Nouwens A, Carroll BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. PNAS 107:12883–12888. https://doi.org/10.1073/pnas.1001085107
doi: 10.1073/pnas.1001085107
Lowe TM, Chan PP (2016) tRNAscan-SE on-line: search and contextual analysis of transfer RNA genes. Nucleic Acids Res 44:W54-57
doi: 10.1093/nar/gkw413
pubmed: 27174935
pmcid: 4987944
Mansuripur M (2002) DNA, human memory, and the storage technology of the 21st century. In: T. Hurst, & S. Kobayashi (Eds) Proceedings of SPIE - The International Society for Optical Engineering (Vol. 4342, pp. 1–29). https://doi.org/10.1117/12.453368
O’Donoghue P, Luthey-Schulten Z (2003) On the evolution of structure in aminoacyl-tRNA synthetases. Microbiol Mol Biol Rev 67:550–573. https://doi.org/10.1128/MMBR.67.4.550-573.2003
doi: 10.1128/MMBR.67.4.550-573.2003
pubmed: 14665676
pmcid: 309052
Oakeson KF, Wagner JM, Mendenhall M, Rohrwasser A, Atkinson-Dunn R (2017) Bioinformatic analyses of whole-genome sequence data in a public health laboratory. Emerg Infect Dis 23(9):1441–1445. https://doi.org/10.3201/eid2309.170416
doi: 10.3201/eid2309.170416
pubmed: 28820135
pmcid: 5572866
Outten FW, Theil EC (2009) Iron-based redox switches in biology. Antioxid Redox Signal 11:1029–1046. https://doi.org/10.1089/ars.2008.2296
doi: 10.1089/ars.2008.2296
pubmed: 19021503
pmcid: 2842161
Pak D, Root-Bernstein R, Burton ZF (2017) tRNA structure and evolution and standardization to the three nucleotide genetic code. Transcription 8(4):205–219. https://doi.org/10.1080/21541264.2017.1318811
Pinos S, Pontarotti P, Raoult D, Baudoin JP, Pagnier I (2016) Compartmentalization in PVC superphylum: evolution and impact. Biol Direct 11:38. https://doi.org/10.1186/s13062-016-0144-3
doi: 10.1186/s13062-016-0144-3
pubmed: 27507008
pmcid: 4977879
Pressman A, Blanco C, Chen IA (2015) The RNA world as a model system to study the origin of life. Curr Biol 25(19):R953-963. https://doi.org/10.1016/j.cub.2015.06.016
doi: 10.1016/j.cub.2015.06.016
pubmed: 26439358
Rivas-Marín E, Devos DP (2018) The paradigms they are a-changin’: past, present and future of PVC bacteria research. Antonie Van Leeuwenhoek 111(6):785–799. https://doi.org/10.1007/s10482-017-0962-z
doi: 10.1007/s10482-017-0962-z
pubmed: 29058138
Rivas-Marín E, Canosa I, Devos DP (2016) Evolutionary cell biology of division mode in the bacterial Planctomycetes-Verrucomicrobia-Chlamydiae superphylum. Front Microbiol 7:1964. https://doi.org/10.3389/fmicb.2016.01964
doi: 10.3389/fmicb.2016.01964
pubmed: 28018303
pmcid: 5147048
Root-Bernstein R, Kimb Y, Sanjay A, Burton ZF (2016) tRNA evolution from the proto-tRNA minihelix world. Transcription 7(5):153–163. https://doi.org/10.1080/21541264.2016.1235527
doi: 10.1080/21541264.2016.1235527
pubmed: 27636862
pmcid: 5066508
Scriven M (1959) Explanation and prediction in evolutionary theory. Science 130(3374):477–482. https://doi.org/10.1126/science.130.3374.477
doi: 10.1126/science.130.3374.477
pubmed: 14444298
Smith TF, Hartman H (2015) The evolution of class II aminoacyl-tRNA synthetases and the first code. FEBS Lett 589:3499–3507. https://doi.org/10.1016/j.febslet.2015.10.006
doi: 10.1016/j.febslet.2015.10.006
pubmed: 26472323
Staley JT (2017) Domain cell theory supports the independent evolution of the eukarya, bacteria and archaea and the nuclear compartment commonality hypothesis. Open Biol 7:170041. https://doi.org/10.1098/rsob.170041
doi: 10.1098/rsob.170041
pubmed: 28659382
pmcid: 5493775
van Niftrik L, Devos DP (2017) Editorial: Planctomycetes-Verrucomicrobia-Chlamydiae bacterial superphylum: new model organisms for evolutionary cell biology. Front Microbiol 8:1458. https://doi.org/10.3389/fmicb.2017.01458
doi: 10.3389/fmicb.2017.01458
pubmed: 28824586
pmcid: 5539593
WagnerM HM (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17(3):241–249. https://doi.org/10.1016/j.copbio.2006.05.005
doi: 10.1016/j.copbio.2006.05.005
Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin MF (2016) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1:16116. https://doi.org/10.1038/nmicrobiol.2016.116
doi: 10.1038/nmicrobiol.2016.116
pubmed: 27562259
Williams MB (1982) The importance of prediction testing in evolutionary biology. Erkenntnis 17:291. https://doi.org/10.1007/BF00182671
doi: 10.1007/BF00182671
Williamson PO, Minter CIJ (2019) Exploring PubMed as a reliable resource for scholarly communications services. J Med Libr Assoc 107(1):16–29. https://doi.org/10.5195/jmla.2019.433
doi: 10.5195/jmla.2019.433
Wolf YI, Koonin EV (2007) On the origin of the translation system and the genetic code in the RNA world by means of natural selection, exaptation, and subfunctionalization. Biol Direct 2:14. https://doi.org/10.1186/1745-6150-2-14
doi: 10.1186/1745-6150-2-14
pubmed: 17540026
pmcid: 1894784
Wong JTF, Ng SK, Mat WK, Hu T, Xue H (2016) Coevolution theory of the genetic code at age forty: pathway to translation and synthetic life. Life 6(1):12. https://doi.org/10.3390/life6010012
doi: 10.3390/life6010012
pubmed: 26999216
pmcid: 4810243