The overlooked evolutionary dynamics of 16S rRNA revises its role as the "gold standard" for bacterial species identification.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 Apr 2024
20 Apr 2024
Historique:
received:
13
11
2023
accepted:
12
04
2024
medline:
21
4
2024
pubmed:
21
4
2024
entrez:
20
4
2024
Statut:
epublish
Résumé
The role of 16S rRNA has been and largely remains crucial for the identification of microbial organisms. Although 16S rRNA could certainly be described as one of the most studied sequences ever, the current view of it remains somewhat ambiguous. While some consider 16S rRNA to be a variable marker with resolution power down to the strain level, others consider them to be living fossils that carry information about the origin of domains of cellular life. We show that 16S rRNA is clearly an evolutionarily very rigid sequence, making it a largely unique and irreplaceable marker, but its applicability beyond the genus level is highly limited. Interestingly, it seems that the evolutionary rigidity is not driven by functional constraints of the sequence (RNA-protein interactions), but rather results from the characteristics of the host organism. Our results suggest that, at least in some lineages, Horizontal Gene Transfer (HGT) within genera plays an important role for the evolutionary non-dynamics (stasis) of 16S rRNA. Such genera exhibit an apparent lack of diversification at the 16S rRNA level in comparison to the rest of a genome. However, why it is limited specifically and solely to 16S rRNA remains enigmatic.
Identifiants
pubmed: 38643216
doi: 10.1038/s41598-024-59667-3
pii: 10.1038/s41598-024-59667-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9067Subventions
Organisme : Ministry of Defence, Czech Republic
ID : MO1012
Informations de copyright
© 2024. The Author(s).
Références
Sanger, F., Nicklen, S. & Coulson, A. R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. 74, 5463–5467 (1977).
pubmed: 271968
pmcid: 431765
doi: 10.1073/pnas.74.12.5463
Heather, J. M. & Chain, B. The sequence of sequencers: The history of sequencing DNA. Genomics 107, 1–8 (2016).
pubmed: 26554401
doi: 10.1016/j.ygeno.2015.11.003
Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc. Natl. Acad. Sci. 74, 5088–5090 (1977).
pubmed: 270744
pmcid: 432104
doi: 10.1073/pnas.74.11.5088
Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: Proposal for the domains archaea, bacteria, and eucarya. Proc. Natl. Acad. Sci. 87, 4576–4579 (1990).
pubmed: 2112744
pmcid: 54159
doi: 10.1073/pnas.87.12.4576
Anda, M. et al. Bacteria can maintain rRNA operons solely on plasmids for hundreds of millions of years. Nat. Commun. 14(1), 7232 (2023).
pubmed: 37963895
pmcid: 10645730
doi: 10.1038/s41467-023-42681-w
Olsen, G. J. & Woese, C. R. Ribosomal RNA: A key to phylogeny. FASEB J. 7, 113–123 (1993).
pubmed: 8422957
doi: 10.1096/fasebj.7.1.8422957
Teng, F. et al. Impact of DNA extraction method and targeted 16S-rRNA hypervariable region on oral microbiota profiling. Sci. Rep. 8 (2018).
Johnson, J. S. et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat. Commun. 10 (2019).
Jeong, J. et al. The effect of taxonomic classification by full-length 16S rRNA sequencing with a synthetic long-read technology. Sci. Rep. 11 (2021).
Hugenholtz, P., Chuvochina, M., Oren, A., Parks, D. H. & Soo, R. M. Prokaryotic taxonomy and nomenclature in the age of big sequence data. ISME J. 15, 1879–1892 (2021).
pubmed: 33824426
pmcid: 8245423
doi: 10.1038/s41396-021-00941-x
Dueholm, M. K. D. et al. MiDAS 4: A global catalogue of full-length 16S rRNA gene sequences and taxonomy for studies of bacterial communities in wastewater treatment plants. Nat. Commun. 13 (2022).
Zhang, J. et al. Phylogenetic analysis of Arthrospira strains from Ordos based on 16S rRNA. Sci. Rep. 12 (2022).
Chen, Z. et al. Impact of preservation method and 16S rRNA hypervariable region on gut microbiota profiling. mSystems 4, 13 (2019).
doi: 10.1128/mSystems.00271-18
Shang, S., Chen, G., Wu, Y., Du, L. & Zhao, Z. Rapid diagnosis of bacterial sepsis with PCR amplification and microarray hybridization in 16S rRNA gene. Pediatr. Res. 58, 143–148 (2005).
pubmed: 15985688
doi: 10.1203/01.PDR.0000169580.64191.8B
Church, D. L. et al. Performance and application of 16S rRNA gene cycle sequencing for routine identification of bacteria in the clinical microbiology laboratory. Clin. Microbiol. Rev. 33(4), 10–1128 (2020).
doi: 10.1128/CMR.00053-19
Cuénod, A., Foucault, F., Pflüger, V. & Egli, A. Factors associated with MALDI-TOF mass spectral quality of species identification in clinical routine diagnostics. Front. Cell. Infect. Microbiol. 11 (2021).
Alizadeh, M. et al. MALDI–TOF mass spectroscopy applications in clinical microbiology. Adv. Pharmacol. Pharmaceut. Sci. 2021, 1–8 (2021).
Singhal, N., Kumar, M., Kanaujia, P. K. & Virdi, J. S. MALDI–TOF mass spectrometry: An emerging technology for microbial identification and diagnosis. Front. Microbiol. 6 (2015).
Lee, I., Ouk Kim, Y., Park, S. C. & Chun, J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evolut. Microbiol. 66, 1100–1103 (2016).
doi: 10.1099/ijsem.0.000760
Miyazaki, K. & Tomariguchi, N. Occurrence of randomly recombined functional 16S rRNA genes in Thermus thermophilus suggests genetic interoperability and promiscuity of bacterial 16S rRNAs. Sci. Rep. 9, 11233 (2019).
pubmed: 31375780
pmcid: 6677816
doi: 10.1038/s41598-019-47807-z
Jain, R., Rivera, M. C. & Lake, J. A. Horizontal gene transfer among genomes: The complexity hypothesis. Proc. Natl. Acad. Sci. 96, 3801–3806 (1999).
pubmed: 10097118
pmcid: 22375
doi: 10.1073/pnas.96.7.3801
Tian, R. M., Cai, L., Zhang, W. P., Cao, H. L. & Qian, P.-Y. Rare events of intragenus and intraspecies horizontal transfer of the 16S rRNA gene. Genome Biol. Evolut. 7, 2310–2320 (2015).
doi: 10.1093/gbe/evv143
Kitahara, K., Yasutake, Y. & Miyazaki, K. Mutational robustness of 16S ribosomal RNA, shown by experimental horizontal gene transfer in Escherichia coli. Proc. Natl. Acad. Sci. 109, 19220–19225 (2012).
pubmed: 23112186
pmcid: 3511107
doi: 10.1073/pnas.1213609109
Schadt, E. E., Turner, S. & Kasarskis, A. A window into third-generation sequencing. Hum. Mol. Genet. 19, R227–R240 (2010).
pubmed: 20858600
doi: 10.1093/hmg/ddq416
Colnaghi, M., Lane, N. & Pomiankowski, A. Repeat sequences limit the effectiveness of lateral gene transfer and favored the evolution of meiotic sex in early eukaryotes. Proc. Natl. Acad. Sci. 119, 220504119 (2022).
doi: 10.1073/pnas.2205041119
Kitahara, K. & Miyazaki, K. Revisiting bacterial phylogeny. Mobile genetic. Elements 3, e24210 (2013).
Hassler, H. B. et al. Phylogenies of the 16S rRNA gene and its hypervariable regions lack concordance with core genome phylogenies. Microbiome 10, 104 (2022).
pubmed: 35799218
pmcid: 9264627
doi: 10.1186/s40168-022-01295-y
Caudill, M. T. & Brayton, K. A. The use and limitations of the 16S rRNA sequence for species classification of anaplasma samples. Microorganisms 10, 605 (2022).
pubmed: 35336180
pmcid: 8949108
doi: 10.3390/microorganisms10030605
Higgs, P. G. Chemical evolution and the evolutionary definition of life. J. Mol. Evolut. 84, 225–235 (2017).
doi: 10.1007/s00239-017-9799-3
Roberts, E., Sethi, A., Montoya, J., Woese, C. R. & Luthey-Schulten, Z. Molecular signatures of ribosomal evolution. Proc. Natl. Acad. Sci. 105, 13953–13958 (2008).
pubmed: 18768810
pmcid: 2528867
doi: 10.1073/pnas.0804861105
Hsiao, C., Mohan, S., Kalahar, B. K. & Williams, L. D. Peeling the onion: Ribosomes are ancient molecular fossils. Mol. Biol. Evolut. 26, 2415–2425 (2009).
doi: 10.1093/molbev/msp163
Bowman, J. C., Petrov, A. S., Frenkel-Pinter, M., Penev, P. I. & Williams, L. D. Root of the tree: The significance, evolution, and origins of the ribosome. Chem. Rev. 120, 4848–4878 (2020).
pubmed: 32374986
doi: 10.1021/acs.chemrev.9b00742
Pietromonaco, S. F., Hessler, R. A. & O’Brien, T. W. Evolution of proteins in mammalian cytoplasmic and mitochondrial ribosomes. J. Mol. Evolut. 24, 110–117 (1986).
doi: 10.1007/BF02099958
O’Brien, T. Properties of human mitochondrial ribosomes. IUBMB Life (International Union of Biochemistry and Molecular Biology: Life) 55, 505–513 (2003).
pubmed: 14658756
doi: 10.1080/15216540310001626610
Petrov, A. S. et al. Structural patching fosters divergence of mitochondrial ribosomes. Mol. Biol. Evolut. 36, 207–219 (2018).
doi: 10.1093/molbev/msy221
Kim, M., Oh, H. S., Park, S. C. & Chun, J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evolut. Microbiol. 64, 346–351 (2014).
doi: 10.1099/ijs.0.059774-0
Baldauf, S. L. Phylogeny for the faint of heart: A tutorial. Trends Genet. 19, 345–351 (2003).
pubmed: 12801728
doi: 10.1016/S0168-9525(03)00112-4
Koonin, E. V. Systemic determinants of gene evolution and function. Mol. Syst. Biol. 1 (2005).
Alvarez-Ponce, D., Sabater-Muñoz, B., Toft, C., Ruiz-González, M. X. & Fares, M. A. Essentiality is a strong determinant of protein rates of evolution during mutation accumulation experiments in Escherichia coli. Genome Biol. Evolut. 8, 2914–2927 (2016).
doi: 10.1093/gbe/evw205
Acinas, S. G., Marcelino, L. A., Klepac-Ceraj, V. & Polz, M. F. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J. Bacteriol. 186, 2629–2635 (2004).
pubmed: 15090503
pmcid: 387781
doi: 10.1128/JB.186.9.2629-2635.2004
Mano, S. & Innan, H. The evolutionary rate of duplicated genes under concerted evolution. Genetics 180, 493–505 (2008).
pubmed: 18757936
pmcid: 2535699
doi: 10.1534/genetics.108.087676
Espejo, R. T. & Plaza, N. Multiple ribosomal RNA operons in bacteria; their concerted evolution and potential consequences on the rate of evolution of their 16S rRNA. Front. Microbiol. 9, 1232 (2018).
pubmed: 29937760
pmcid: 6002687
doi: 10.3389/fmicb.2018.01232
Kimura, M. Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. Genet. Res. 11, 247–270 (1968).
pubmed: 5713805
doi: 10.1017/S0016672300011459
Ohta, T. The nearly neutral theory of molecular evolution. Ann. Rev. Ecol. Syst. 23, 263–286 (1992).
doi: 10.1146/annurev.es.23.110192.001403
Bosshard, L., Peischl, S., Ackermann, M. & Excoffier, L. Dissection of the mutation accumulation process during bacterial range expansions. BMC Genomics 21 (2020).
Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Mol. Phylogenet. Evolut. 26, 1–7 (2003).
doi: 10.1016/S1055-7903(02)00326-3
van Wolferen, M., Ajon, M., Driessen, A. J. M. & Albers, S.-V. How hyperthermophiles adapt to change their lives: DNA exchange in extreme conditions. Extremophiles 17, 545–563 (2013).
pubmed: 23712907
doi: 10.1007/s00792-013-0552-6
Vos, M. The evolution of bacterial pathogens in the Anthropocene. Infect. Genet. Evolut. 86, 104611 (2020).
doi: 10.1016/j.meegid.2020.104611
Sessions, S. K. Genome size. In Brenner’s Encyclopedia of Genetics. 301–305 https://doi.org/10.1016/b978-0-12-374984-0.00639-2 (2013).
Deagle, B. E., Jarman, S. N., Coissac, E., Pompanon, F. & Taberlet, P. DNA metabarcoding and the cytochrome c oxidase subunit I marker: Not a perfect match. Biol. Lett. 10(9), 20140562 (2014).
pubmed: 25209199
pmcid: 4190964
doi: 10.1098/rsbl.2014.0562
Sato, Y., Miya, M., Fukunaga, T., Sado, T. & Iwasaki, W. MitoFish and MiFish pipeline: A mitochondrial genome database of fish with an analysis pipeline for environmental DNA metabarcoding. Mol. Biol. Evolut. 35(6), 1553–1555 (2018).
doi: 10.1093/molbev/msy074
Scornavacca, C. & Galtier, N. Incomplete lineage sorting in mammalian phylogenomics. Syst. Biol. syw082 (2016).
Kurylo, C. M. et al. Endogenous rRNA sequence variation can regulate stress response gene expression and phenotype. Cell Rep. 25(1), 236–248 (2018).
pubmed: 30282032
pmcid: 6312700
doi: 10.1016/j.celrep.2018.08.093
Ferretti, M. B. & Karbstein, K. Does functional specialization of ribosomes really exist?. RNA 25(5), 521–538 (2019).
pubmed: 30733326
pmcid: 6467006
doi: 10.1261/rna.069823.118
Barna, M. Ribosomes take control. Proc. Natl. Acad. Sci. 110(1), 9–10 (2013).
pubmed: 23243144
doi: 10.1073/pnas.1218764110
Lim, J. Y., Yoon, J. W. & Hovde, C. J. A brief overview of Escherichia coli O157: H7 and its plasmid O157. J. Microbiol. Biotechnol. 20(1), 5 (2010).
pubmed: 20134227
doi: 10.4014/jmb.0908.08007
Ameer, M. A., Wasey, A., & Salen, P.. Escherichia coli (E Coli 0157 H7) (2018).
Nearing, J. T., Comeau, A. M. & Langille, M. G. I. Identifying biases and their potential solutions in human microbiome studies. Microbiome 9, 113 (2021).
pubmed: 34006335
pmcid: 8132403
doi: 10.1186/s40168-021-01059-0
Santoyo, G. & Romero, D. Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol. Rev. 29(2), 169–183 (2005).
pubmed: 15808740
doi: 10.1016/j.femsre.2004.10.004
Dover, G. Molecular drive. Trends Genet. 18(11), 587–589 (2002).
pubmed: 12414190
doi: 10.1016/S0168-9525(02)02789-0